Root architecture varies widely between species, and even between ecotypes of the same species, despite the strong conservation of the coding portion of their genomes. By contrast, non-coding RNAs evolve rapidly between ecotypes and may control their differential responses to the environment, since several long non-coding RNAs (lncRNAs) are known to quantitatively regulate gene expression. Roots from Columbia (Col) and Landsberg erecta (Ler) ecotypes respond differently to phosphate starvation. Here, we compared transcriptomes (mRNAs, lncRNAs, and small RNAs) of root tips from these two ecotypes during early phosphate starvation. We identified thousands of lncRNAs that were largely conserved at the DNA level in these ecotypes. In contrast to coding genes, many lncRNAs were specifically transcribed in one ecotype and/or differentially expressed between ecotypes independent of phosphate availability. We further characterized these ecotype-related lncRNAs and studied their link with siRNAs. Our analysis identified 675 lncRNAs differentially expressed between the two ecotypes, including antisense RNAs targeting key regulators of root-growth responses. Mis-regulation of several intergenic lncRNAs showed that at least two ecotype-related lncRNAs regulate primary root growth in Col. RNA-seq analysis following the deregulation of the lncRNA NPC48 revealed a potential link with root growth and transport functions. This exploration of the non-coding transcriptome identified ecotype-specific lncRNAs-mediated regulation in root apexes. The non-coding genome may harbor further mechanisms involved in ecotype adaptation of roots to different soil environments.